Abstract
SummaryThe myosin II activator Rho-kinase (Rok) is planar polarized at the tissue boundary of the Drosophila embryonic salivary gland placode through a negative regulation by the apical polarity protein Crumbs that is anisotropically localized at the boundary. However, in inner cells of the placode, both Crumbs and Rok are isotropically enriched at junctions. We propose that modulation of Rok membrane residence time by Crumbs’ downstream effectors can reconcile both behaviors. Using FRAP combined with in silico simulations, we find that the lower membrane dissociation rate (koff) of Rok at the tissue boundary with low Crumbs explains this boundary-specific effect. The S/T kinase Pak1, recruited by Crumbs and Cdc42, negatively affects Rok membrane association in vivo and in vitro can phosphorylate Rok near the pleckstrin homology (PH) domain that mediates membrane association. These data reveal an important mechanism of the modulation of Rok membrane residence time via affecting the koff that may be widely employed during tissue morphogenesis.
Highlights
Tissues arise during development through specification of primordia that will initiate morphogenetic movements (Castelli-Gair Hombria and Bovolenta, 2016)
This seems to be in part achieved through an increased tension at the compartment boundary that coincides with junctional accumulation of actomyosin into a seemingly supracellular structure, a so-called actomyosin cable (Roper, 2013)
We have previously identified that an actomyosin cable is positioned at the boundary of the salivary gland placode in the Drosophila embryo (Roper, 2012)
Summary
Tissues arise during development through specification of primordia that will initiate morphogenetic movements (Castelli-Gair Hombria and Bovolenta, 2016). We know from studies in the Drosophila early embryonic epidermis as well as in larval wing discs that differently fated compartments are physically clearly segregated, and cell mixing across compartment boundaries is restricted (Dahmann and Basler, 1999; Tepass et al, 2002). In both tissues, this seems to be in part achieved through an increased tension at the compartment boundary that coincides with junctional accumulation of actomyosin into a seemingly supracellular structure, a so-called actomyosin cable (Roper, 2013). Actomyosin-based compartment boundaries are not restricted to invertebrates but have been found in vertebrates, with key examples being the rhombomere boundaries in the mammalian hindbrain (Calzolari et al, 2014) as well as the neural plate-ectoderm boundary during neurulation (Galea et al, 2017)
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